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Nearly half a century ago insect herbivores were found to induce the formation of green islands by manipulating cytokinin (CK) levels. However, the response of the CK pathway to attack by chewing insect herbivores remains unclear. Here, we characterize the CK pathway of  Nicotiana attenuata  (Torr. ex S. Wats.) and its response to wounding and perception of herbivore‐associated molecular patterns (HAMPs). We identified 44 genes involved in CK biosynthesis, inactivation, degradation, and signaling. Leaf wounding rapidly induced transcriptional changes in multiple genes throughout the pathway, as well as in the levels of CKs, including isopentenyladenosine and  cis ‐zeatin riboside; perception of HAMPs present in the oral secretions (OS) of the specialist herbivore  Manduca sexta  amplified these responses. The jasmonate pathway, which triggers many herbivore‐induced processes, was not required for these HAMP‐triggered changes, but rather suppressed the CK responses. Interestingly CK pathway changes were observed also in systemic leaves in response to wounding and OS application indicating a role of CKs in mediating long distance systemic processes in response to herbivory. Since wounding and grasshopper OS elicited similar accumulations of CKs in  Arabidopsis thaliana  L., we propose that CKs are integral components of wounding and HAMP‐triggered responses in many plant species.

Cytokinin levels and signaling respond to wounding and the perception of herbivore elicitors in Nicotiana attenuata